The emergence of Schmallenberg virus across Culicoides communities and ecosystems in Europe

Schmallenberg virus (SBV), a novel arboviral pathogen, has emerged and spread across Europe since 2011 inflicting congenital deformities in the offspring of infected adult ruminants. Several species of Culicoides biting midges (Diptera: Ceratopogonidae) have been implicated in the transmission of SBV through studies conducted in northern Europe. In this study Culicoides from SBV outbreak areas of mainland France and Italy (Sardinia) were screened for viral RNA. The role of both C. obsoletus and the Obsoletus complex (C. obsoletus and C. scoticus) in transmission of SBV were confirmed in France and SBV was also discovered in a pool of C. nubeculosus for the first time, implicating this species as a potential vector. While collections in Sardinia were dominated by C. imicola, only relatively small quantities of SBV RNA were detected in pools of this species and conclusive evidence of its potential role in transmission is required.     

Evaluating the protective efficacy of a trivalent vaccine containing Akabane virus,Aino virus and Chuzan virus against Schmallenberg virus infection

Schmallenberg virus (SBV), an arthropod borne pathogen, spread rapidly throughout the majority of Europe since 2011. It can cause a febrile disease, milk drop, diarrhea, and fetal malformation in ruminants. SBV, a member of the Simbu serogroup within the genus Orthobunyavirus, is closely related to Akabane virus (AKAV) and Aino virus (AINOV) among others. In the present study, 4 Holstein-Friesian calves were immunized twice four weeks apart with a multivalent, inactivated vaccine against AKAV and AINOV. Another 4 calves were kept as unvaccinated controls. All animals were clinically, serologically and virologically examined before and after challenge infection with SBV. AKAV- and AINOV-specific neutralizing antibodies were detected one week before challenge infection, while SBV-specific antibodies were detectable only thereafter. SBV genome was detected in all vaccinated animals and 3 out of 4 controls in serum samples taken after challenge infection. In conclusion, the investigated vaccine was not able to prevent an SBV-infection. Thus, vaccines for other related Simbu serogroup viruses can not substitute SBV-specific vaccines as an instrument for disease control.     

Single immunization with an inactivated vaccine protects sheep from Schmallenberg virus infection

The arthropod-borne Schmallenberg virus (SBV), family Orthobunyaviridae, emerged in Europe in 2011. SBV is associated with a mild disease in adult ruminants but fetal malformation after an infection during a critical phase of pregnancy. A number of inactivated vaccines have been developed; their efficacy after two injections was demonstrated. To make the vaccination of sheep more efficient and economic the effect of a single immunization with one of these vaccines was investigated in the present study. Five vaccinated sheep and five additional control sheep were inoculated with SBV three weeks after vaccination and the results of a competitive ELISA, a standard microneutralization test and an SBV-specific real-time RT-PCR confirmed vaccine efficacy by demonstrating complete inhibition of viral replication in immunized animals.     

Inferences about the transmission of Schmallenberg virus within and between farms

In the summer of 2011 Schmallenberg virus (SBV), a Culicoides-borne orthobunyavirus, emerged in Germany and The Netherlands and subsequently spread across much of Europe. To draw inferences about the transmission of SBV we have developed two models to describe its spread within and between farms. The within-farm model was fitted to seroprevalence data for cattle and sheep farms in Belgium and The Netherlands, with parameters estimated using approximate Bayesian computation. Despite the short duration of viraemia in cattle and sheep (mean of 3–4 days) the within-farm seroprevalence can reach high levels (mean within-herd seroprevalence >80%), largely because the probability of transmission from host to vector is high (14%) and SBV is able to replicate quickly (0.03 per day-degree) and at relatively low temperatures (threshold for replication: 12.3 °C). Parameter estimates from the within-farm model were then used in a separate between-farm model to simulate the regional spread of SBV. This showed that the rapid spread of SBV at a regional level is primarily a consequence of the high probability of transmission from host to vector and the temperature requirements for virus replication. Our results, obtained for a region of the UK in a typical year with regard to animal movements, indicate that there is no need to invoke additional transmission mechanisms to explain the observed patterns of rapid spread of SBV in Europe. Moreover, the imposition of movement restrictions, even a total movement ban, has little effect on the spread of SBV at this scale.     

Schmallenberg virus epidemic: Impact on milk production,reproductive performance and mortality in dairy cattle in the Netherlands and Kleve district,Germany

Schmallenberg virus (SBV), a novel orthobunyavirus that rapidly spread throughout north-western Europe in 2011, caused congenital malformations in lambs and goat kids (Van den Brom et al., 2012) and newborn calves (Hoffmann et al., 2012). The impact of the SBV epidemic seemed limited however, in terms of the number of affected herds with malformed offspring (European Food Safety Authority, 2012b). Nevertheless, little is known with regard to the overall within-herd impact of SBV infection. The objective of the current study was to quantify the impact of the 2011 SBV epidemic on the productivity of dairy cattle in the Netherlands and the district of Kleve, Germany.     

Development and evaluation of an indirect enzyme-linked immunosorbent assay for serological detection of Schmallenberg virus antibodies in ruminants using whole virus antigen

Background

In late 2011, a new Orthobunyavirus of the Simbu serogroup named Schmallenberg virus (SBV) emerged in continental Europe. The virus is transmitted by hematophagous arthropods, with the Culicoides species as, so far known, main vectors. Infection with the virus can cause clinical signs in adult ruminants including diarrhea, fever and reduced milk production. Transplacental infection of the developing fetus can lead to malformations of varying severity. To assess seroprevalence of SBV in Sweden an indirect enzyme-linked immunosorbent assay (ELISA) was established in connection with the surveys. Here, we describe the development and evaluation of the indirect ELISA, based on whole virus as the coating antigen and a monoclonal antibody for the detection of antibodies to SBV in ruminant sera. The evaluation includes comparison between the in-house ELISA, virus neutralization test and an indirect commercial ELISA.

Results

The optimal working dilutions of antigens and conjugate were estimated with checkerboard titrations. Comparative studies, including ROC analyses, were used for the selection of an optimal cut-off (S/P value = sample value as percentage of positive control value). With an estimated S/P value of 15% the whole virus ELISA showed a specificity of 100% and a sensitivity of 99.19% compared to virus neutralization test (VNT) and with a good consistency as shown in reproducibility and variability experiments. Furthermore, the comparison of our whole virus indirect ELISA to an indirect ELISA with a SBV nucleoprotein antigen, demonstrated a higher sensitivity of our test.

Conclusion

The indirect whole virus ELISA described in this paper is a readily available test for serological analysis of SBV antibodies. Since this in-house ELISA demonstrates a specificity and sensitivity comparable to virus neutralization test and also shows a higher sensitivity compared to commercially available indirect ELISA, it is a useful alternative for surveillance and screening purposes of SBV.     

Evidence of excretion of Schmallenberg virus in bull semen

Schmallenberg virus (SBV) is a novel orthobunyavirus, discovered in Germany in late 2011. It mainly infects cattle, sheep and goats and could lead to congenital infection, causing abortion and fetal abnormalities. SBV is transmitted by biting midges from the Culicoides genus and there is no evidence that natural infection occurs directly between ruminants. Here, we could detect SBV RNA in infected bull semen using qRT-PCR (three bulls out of seven tested positive; 29 positive semen batches out of 136). We also found that highly positive semen batches from SBV infected bulls can provoke an acute infection in IFNAR^-/- mice, suggesting the potential presence of infectious virus in the semen of SBV infected bulls.     

Rapid spread and association of Schmallenberg virus with ruminant abortions and foetal death in Austria in 2012/2013

Schmallenberg virus (SBV) has emerged in summer–autumn 2011 in north-western Europe. Since then, SBV has been continuously spreading over Europe, including Austria, where antibodies to SBV, as well as SBV genome, were first detected in autumn 2012. This study was performed to demonstrate the dynamics of SBV spread within Austria, after its probable first introduction in summer 2012. True seroprevalence estimates for cattle and small ruminates were calculated to demonstrate temporal and regional differences of infection. Furthermore, the probability of SBV genome detection in foetal tissues of aborted or stillborn cattle and small ruminants as well as in allantoic fluid samples from cows with early foetal losses was retrospectively assessed.     

Schmallenberg virus—Two years of experiences

In autumn 2011, a novel species of the genus Orthobunyavirus of the Simbu serogroup was discovered close to the German/Dutch border and named Schmallenberg virus (SBV). Since then, SBV has caused a large epidemic in European livestock. Like other viruses of the Simbu serogroup, SBV is transmitted by insect vectors. Adult ruminants may show a mild transient disease, while an infection during a critical period of pregnancy can lead to severe congenital malformation, premature birth or stillbirth. The current knowledge about the virus, its diagnosis, the spread of the epidemic, the impact and the possibilities for preventing infections with SBV is described and discussed.     

Schmallenberg virus challenge models in cattle: infectious serum or culture-grown virus?

Schmallenberg virus (SBV), discovered in Europe in 2011, causes mild transient disease in adult ruminants, but fetal infection can lead to severe malformation in cattle, sheep and goats.To elucidate the pathogenesis of this novel orthobunyavirus, considerable efforts are required. A reliable and standardized infection model is essential for in vivo studies. In the present study, two groups of four cattle were inoculated with either serum passaged in cattle only or cell culture-grown virus. The replication of culture-grown SBV in cattle was reduced compared to virus inoculated via infectious serum. In a second experiment, the infectious serum was titrated in calves; the tested batch contained 10^2.83 infectious doses per mL. Hence, serum-borne virus that was only passaged in the natural host is a suitable option for a standardized SBV infection model.     

The Schmallenberg virus epidemic in Europe—2011–2013

During the Schmallenberg virus (SBV) epidemic, the European Food Safety Authority (EFSA) collected data on SBV occurrence across Europe in order to provide an assessment of spread and impact. By May 2013, twenty-nine countries were reporting to EFSA and twenty-two countries had reported cases of SBV. The total number of SBV herds reported was 13,846 and the number of SBV laboratory confirmed herds was 8730. The surveillance activities were based on the detection of SBV clinical cases (either adults or newborns). Malformation in newborns was the most commonly reported clinical sign of SBV-infection. All countries were able to provide the date when the first suspicion of SBV in the herd was reported and nineteen could report the location of the herd at a regional level. This allowed the spread of SBV in Europe to be measured both temporally and spatially. The number of SBV confirmed herds started to increase in December 2011 and two peaks were observed in 2012 (February and May). Confirmed herds continued to be reported in 2012 and into 2013. An increase during winter 2012 and spring 2013 was again observed, but the number of confirmed herds was lower than in the previous year. SBV spread rapidly throughout Europe from the initial area of detection. SBV was detected above the latitude of 60° North, which exceeds the northern expansion observed during the bluetongue virus serotype 8 epidemic in 2006–2009. The impact of SBV was calculated as ratio of the number of herds with at least one malformed SBV positive foetus and the total number of herds in this region. The 75th percentile of the malformations ratio in the various affected countries for the whole reporting period was below 1% and 3% for cattle and sheep herds, respectively. International data collection on emerging diseases represents a challenge as the nature of available data, data quality and the proportion of reported cases may vary widely between affected countries. Surveillance activities on emerging animal diseases are often structured only for case detection making the estimation of infection/diseases prevalence and the investigation of risk factors difficult. The impact of the disease must be determined to allow risk managers to take appropriate decisions. Simple within-herd impact indicators suitable for emerging disease outbreaks should be defined that could be measured as part of routine animal health surveillance programmes and allow for rapid and reliable impact assessment of emerging animal health diseases.     

Description of the first Schmallenberg disease outbreak in Spain and subsequent virus spreading in domestic ruminants

Schmallenberg disease (SBD) is an emerging disease transmitted mainly among ruminant species by biting midges of the genus Culicoides. Since the Schmallenberg virus (SBV) was first identified in Germany in late 2011, it rapidly spread to other European countries. The aims of the present study were to describe the first SBD outbreak in Spain and to assess the spread and risk factors associated with SBV infection in domestic ruminants from nearby farms during the following year. In March 2012, one malformed stillborn lamb from a sheep farm located in Cordoba province (Southern Spain) was subjected to necropsy. Pathological compatible lesions and molecular analyses confirmed the first SBV infection in Spain. Afterwards, serum samples from 505 extensively reared domestic ruminants from 29 farms were analysed using both blocking ELISA and virus neutralization test against SBV. The overall seroprevalence was 54.4% (CI_95%: 50.0–58.7). Antibodies were detected in 70.6%, 46.0% and 34.8% of cattle, sheep and goats, respectively. A generalized estimating equation model indicated that the main risk factors associated with SBV infection were: species (cattle), age (adult), and absence of animal insecticide treatment. Pathological and molecular results confirmed the presence of SBV in Spain few months after it was firstly identified in Germany. The seroprevalence detected indicates a widespread circulation of SBV in nearby domestic ruminant farms one year after this first outbreak was reported in Spain. Further studies are warranted to determine the spatio-temporal trend of SBV in domestic ruminants in this country.     

施马伦贝格病毒

施马伦贝格病毒病(Schmallenberg virus,SBV)是一种新发现的动物传染病,因于2011年底在德国施马伦贝格镇首次发现而临时得名,随后蔓延于西欧(包括比利时、法国、德国、荷兰、意大利、卢森堡、西班牙、英国和丹麦),并分别在奥地利、波兰、瑞典和芬兰等国的牛、山羊、绵羊中检测到抗体。遗传分析显示该病毒与布尼亚病毒科(Bunyaviridae)正布尼亚病毒属(Orthobunyavirus)西姆布血清群病毒(Simbu serogroup viruses)的亲缘关系最密切,西姆布血清群病毒是已知的反刍动物病原,可通过节肢动物媒介(蚊、蠓)传播。施马伦贝格病毒病有2种不同的临床症状:成年牛出现短暂轻微/温和的病症(产奶量减少、发热、腹泻)和新生哺乳动物(牛、羊)死产和先天缺陷。因为同群类似的病毒不是人畜共患病病原,也无该病毒致人发病的证据,但现阶段尚不能完全排除。尽管目前没有特效的药物和疫苗,但因已有类似病毒(赤羽病)的疫苗,疫苗接种应是控制该病的可能选项。因施马伦贝格病毒是一种新发现的病毒,许多方面尚不清楚,还有待于进一步研究。     

Serosurveillance of Schmallenberg virus in Switzerland using bulk tank milk samples

Infections with Schmallenberg virus (SBV), a novel Orthobunyavirus transmitted by biting midges, can cause abortions and malformations of newborns and severe symptoms in adults of domestic and wild ruminants. Understanding the temporal and spatial distribution of the virus in a certain territory is important for the control and prevention of the disease. In this study, seroprevalence of antibodies against SBV and the spatial spread of the virus was investigated in Swiss dairy cattle applying a milk serology technique on bulk milk samples. The seroprevalence in cattle herds was significantly higher in December 2012 (99.5%) compared to July 2012 (19.7%). This high between-herd seroprevalence in cattle herds was observed shortly after the first detection of viral infections. Milk samples originating from farms with seropositive animals taken in December 2012 (n = 209; mean 160%) revealed significantly higher S/P% ratios than samples collected in July 2012 (n = 48; mean 103.6%). This finding suggests a high within-herd seroprevalence in infected herds which makes testing of bulk tank milk samples for the identification farms with past exposures to SBV a sensitive method. It suggests also that within-herd transmission followed by seroconversion still occurred between July and December. In July 2012, positive bulk tank milk samples were mainly restricted to the western part of Switzerland whereas in December 2012, all samples except one were positive. A spatial analysis revealed a separation of regions with and without positive farms in July 2012 and no spatial clustering within the regions with positive farms. In contrast to the spatial dispersion of bluetongue virus, a virus that is also transmitted by Culicoides midges, in 2008 in Switzerland, the spread of SBV occurred from the western to the eastern part of the country. The dispersed incursion of SBV took place in the western part of Switzerland and the virus spread rapidly to the remaining territory. This spatial pattern is consistent with the hypothesis that transmission by Culicoides midges was the main way of spreading.     

Preliminary serological evidence for Schmallenberg virus infection in China

Tropical Animal Health and Production - Schmallenberg virus (SBV) is an emerging and rampant arbovirus in Europe, and even Africa and West Asia. Investigating whether SBV existed in new regions or...     

Schmallenberg virus in Dutch dairy herds: Potential risk factors for high within-herd seroprevalence and malformations in calves,and its impact on productivity

In November 2011, the new orthobunyavirus Schmallenberg virus (SBV) was identified in dairy cows that had induced fever, drop in milk production and diarrhoea in the Netherlands (Muskens et al., 2012. Tijdschrift voor Diergeneeskunde 137, 112–115) and a drop in milk production in cows in Northwestern Germany (Hoffmann et al., 2012. Emerging Infectious Diseases 18 (3), 469–472), in August/September 2011. This study aimed at quantifying risk factors for high within-herd prevalence of SBV and SBV-induced malformations in newborn calves in dairy herds in the Netherlands. Additionally, the within-herd impact of SBV infection on mortality rates and milk production was estimated.A case-control design was used, including 75 clinically affected case herds and 74 control herds. Control herds were selected based on absence of malformations in newborn calves and anomalies in reproductive performance. SBV-specific within-herd seroprevalences were estimated. Risk factors for high within-herd SBV seroprevalence (>50%) and the probability of malformed newborn calves in a herd were quantified. In addition, within-herd impact of SBV with regard to milk production and mortality was estimated.Animal-level seroprevalence was 84.4% (95% confidence interval (CI): 70.8–92.3) in case herds and 75.8% (95% CI: 67.5–82.5) in control herds. Control herds that were completely free from SBV were not present in the study. Herds that were grazed in 2011 had an increased odds (OR 9.9; 95% CI: 2.4–41.2)) of a high seroprevalence (>50%) compared to herds that were kept indoors. Also, when grazing was applied in 2011, the odds of malformations in newborn calves tended to be 2.6 times higher compared to herds in which cattle were kept indoors. Incidence of malformations in newborn calves at herd level was associated with both within-herd seroprevalence and clinical expression of the disease in adult cattle.The rate of vertical transmission of SBV to the fetus once a dam gets infected seemed low. A total of 146 stillborn or malformed calves were submitted by 65 farmers during the study period, of which 19 were diagnosed as SBV-positive based on pathological investigation and/or RT-qPCR testing of brain tissue. Based on these results combined with calving data from these herds we roughly estimated that at least 0.5% of the calves born between February and September 2012 have been infected by SBV.A drop in milk production was observed between the end of August 2011 and the first half of September (week 35–36), indicating the acute phase of the epidemic. During a 4-week period in which SBV infection was expected to have occurred, the total loss in milk production in affected dairy herds was around 30–51 kg per cow. SBV had no or limited impact on mortality rates which was as expected given the relatively mild expression of SBV in adult cows and the low incidence of malformations in newborn calves.     

Response to an emerging vector-borne disease: Surveillance and preparedness for Schmallenberg virus

Surveillance for new emerging animal diseases from a European perspective is complicated by the non-harmonised approach across Member States for data capture, recording livestock populations and case definitions. In the summer of 2011, a new vector-borne Orthobunyavirus emerged in Northern Europe and for the first time, a coordinated approach to horizon scanning, risk communication, data and diagnostic test sharing allowed EU Member States to develop early predictions of the disease, its impact and risk management options. There are many different systems in place across the EU for syndromic and scanning surveillance and the differences in these systems have presented epidemiologists and risk assessors with concerns about their combined use in early identification of an emerging disease. The emergence of a new disease always will raise challenging issues around lack of capability and lack of knowledge; however, Schmallenberg virus (SBV) gave veterinary authorities an additional complex problem: the infection caused few clinical signs in adult animals, with no indication of the possible source and little evidence about its spread or means of transmission. This paper documents the different systems in place in some of the countries (Germany and the Netherlands) which detected disease initially and predicted its spread (to the UK) and how information sharing helped to inform early warning and risk assessment for Member States. Microarray technology was used to identify SBV as a new pathogen and data from the automated cattle milking systems coupled with farmer-derived data on reporting non-specific clinical signs gave the first indications of a widespread issue while the UK used meteorological modelling to map disease incursion. The coordinating role of both EFSA and the European Commission were vital as are the opportunities presented by web-based publishing for disseminating information to industry and the public. The future of detecting emerging disease looks more positive in the light of this combined approach in the EU.     

Antibodies to Schmallenberg virus in domestic livestock in Turkey

This, partly retrospective study, was designed to determine the seroprevalence of Schmallenberg virus (SBV), a new Orthobunyavirus first reported in Germany in late 2011, in domestic ruminants from the Middle Black Sea, West, and Southeast regions of Turkey. An indirect enzyme-linked immunosorbent assay was used to screen serum samples collected from slaughterhouse animals between 2006 and 2013. The overall seroprevalence was 335/1,362 (24.5 %) with 325/816 (39.8 %), 5/307 (1.6 %), 3/109 (2.8 %), and 2/130 (1.5 %) recorded in cattle, sheep, goats, and Anatolian water buffalo, respectively. This is the first study to demonstrate the presence of antibodies to SBV in Turkish ruminants; it indicates that cattle are more susceptible to infection than sheep, goats, or buffalo and that exposure of domestic ruminants to SBV in Turkey may have occurred up to 5 years prior to the first recorded outbreak of the disease in 2011.     

A bulk milk tank study to detect evidence of spread of Schmallenberg virus infection in the south-west of Ireland in 2013

Background

Schmallenberg virus (SBV) was first detected in Germany in November 2011. Confirmation of infection in Ireland was reported on October 30^th 2012. The results of a national serological survey carried out in early 2013 suggested that the first introduction of SBV into Ireland probably occurred in the south or southeast of Ireland in the spring or summer of 2012, with subsequent spread eastwards and northwards. It was unclear at that stage whether the virus had survived the winter period and would continue to spread in 2013. The purpose of this study was to monitor the spread of the virus in the mid-west region through the summer and autumn of 2013 using bulk tank milk from selected dairy herds.

Findings

Seventy two dairy farmers were recruited to participate in the bulk milk tank study. Each farmer agreed to collect a bulk tank milk sample on a weekly basis from early June. A total of 988 samples were received between June 5^th and December 3^rd 2013 and these were analysed using an indirect ELISA test. Of the initial set of 72 samples received between June 5^th and July 16^th, nine were positive, one was inconclusive and 62 were negative. By the end of the study in early December 2013 only one new farm turned positive. This was the farm that had initially tested inconclusive.

Conclusion

The study results suggest that the anticipated spread of SBV across Ireland from the south and south-east did not occur during 2013.